Prescription and Effects of Cardiorespiratory Training in Individuals with Intellectual Disability: A Systematic Review

This study aims to systematize effects of cardiorespiratory training (CT) programs in individuals with intellectual disability (ID) and identifying the fundamental and structuring aspects for the prescription of CT. This systematic review was carried out through four databases (Pubmed, Web of Science, Scopus, and SPORTDiscus), considering data from the period between 2013 and 2022. From 257 studies, 12 studies were included in this systematic review. Three studies used interval CT, while seven used continuous CT. Seven were carried out in the population with Down syndrome, while only three were carried out with participants with ID. The CT programs had the following characteristics: duration of 8 to 12 weeks, weekly frequency of three sessions, for 20 to 60 min, the intensity of 50% to 80% of maximal heart rate or 70% to 80% of peak oxygen consumption, using an ergometer cycle or an outdoor walking. The studies reported improvements in cardiorespiratory function, lipid, hemodynamic and metabolic profile, body composition, and neuromuscular and cognitive capacity. This review presents characteristics and recommendations that technicians can follow when structuring, prescribing, and implementing CT programs to individuals with ID.


Introduction
Persons with intellectual disability (ID) are characterized by a deficit of intellectual and adaptive functioning in the conceptual, social, and practical domain [1]. This population is currently considered a social group that demands special attention [2,3] due to their low average life expectancy correlated with the degree of ID [4,5]. Even so, there has been an increase in the average life expectancy of this population over the years [6].
Greater longevity is associated with an increase in comorbidities and health care costs in order to provide adequate care to adults with ID, in particular when they live longer than their parents [7]. The premature aging of individuals with ID starts around the fifth decade of life [8] and also represents serious health concerns [9]. Those health problems are partially attributed to their sedentary lifestyle behaviors, physical inactivity, and the impaired physical fitness associated with several factors such as possible lack of motivation, task understanding, and an unhealthy diet [10]. The sedentary lifestyle ID, of all ages, regardless of gender, race, or ethnicity; (ii) "I" (intervention) corresponded to any CT program performed with ID (including Down syndrome), regardless of the intervention time; (iii) "C" (comparison) corresponded to the comparison between the control group vs. the intervention group or pre and post-intervention; (iv) "O" (outcome) corresponded to CT as the first or second variable under study; (v) "S" (study design) corresponded to randomized controlled clinical trials.

Eligibility Criteria
Studies that provided information regarding the effects of CT interventions on the healthrelated and physical fitness outcomes of individuals with ID were considered eligible if they met the following inclusion criteria: (i) randomized controlled studies; (ii) intervention studies in any type of CT (e.g., continuous or interval) and with any duration (e.g., 8 weeks, 12 weeks, 24 weeks, etc.); (iii) population with ID, in different degrees (e.g., mild, moderate, severe, or profound); (iv) studies with individuals of any race, ethnicity, gender, or age group (since the American College of Sports Medicine (ACSM) also makes no distinction); (v) studies with any number of participants. In turn, all studies with the following characteristics were excluded if: (i) were published before 2013 (considering the first time that the ACSM published a chapter on guidelines for exercise testing and prescription for individuals with ID and Down syndrome in this year [35]); (ii) the research was not written in English; (iii) articles with participants with another type of disability or pathologies (e.g., multiple disabilities); (iv) articles that do not describe the intervention protocol, namely the prescription of CT in the PE program; (v) articles in which the intervention is focused on a sport modality (e.g., soccer); (vi) articles in which the intervention combines several physical abilities (e.g., CT with strength training; CT with nutrition, etc.) (since one intervention may influence the prescription of the other intervention and/or the results may not be caused by the CT); and (vii) articles in which the intervention is not just CT in the same group (example: combined training, CT and nutrition, among others).

Information Sources and Research Strategies
Electronic searches were carried out in the PubMed (title and abstract), Web of Science, Scopus, and SPORTDiscus (tittle/abstract/keywords), encompassing articles published between January 2013 and 9 June 2023 thus encompassing only recent literature and current evidence. At the same time, the period of retreat (2013) of the literature search coincides with the first time that the American College of Sports Medicine-ACSM published a chapter on guidelines for exercise testing and prescription for individuals with ID and Down syndrome [35]. Some medical subject headings (MeSH) descriptors and natural language [36] that we consider to complement the research were used, namely: "aerobic exercise", "aerobic training", "cardio training", "cardiorrespiratory training", "cardiorespiratory training", "cardio exercise", "cardiorrespiratory exercise", "cardiorespiratory exercise", "continuous exercise", "continuous training", "high-intensity interval training", "HIIT", "interval training", "interval exercise", "mental retardation", "intellectual disability", "intellectual disabilities", "intellectual and developmental disabilities", and "Down syndrome", as indicated in Table 1. Table 1. Research strategy.

Search Number
Research Content 1 (aerobic exercise* OR aerobic training* OR cardio training* OR cardiorrespiratory training* OR cardiorespiratory training* OR cardio exercise* OR cardiorrespiratory exercise* OR cardiorespiratory exercise* OR continuous exercise* OR continuous training* OR high-intensity interval training* OR HIIT* OR interval training* OR interval exercise*) AND ("mental retardation" OR "intellectual disability" OR "intellectual disabilities" OR "intellectual and developmental disabilities" OR "Down syndrome")

Selection and Data Collection Process
The aim was to search for intervention studies, based on CT program, regardless of its purpose. The research was carried out autonomously by two authors (MJ and RO) and, after excluding duplicate articles, reading the titles and abstracts, according to the eligibility criteria, the results of both were compared and discussed. When differences arose between these two authors, a third author (JB) was available to collaborate and make a final decision. One of the authors (MJ) downloaded the main information from the articles, namely: authors' names, year of publication, country, aims, participants, type of study, assessment instruments, duration/frequency, exercises, intensities, and main results.

Methodological Quality
The quality assessment of each study was performed based on the PEDro scale and its database, from the Physiotherapy Evidence Database [37,38]. The scale consists of 11 items, which characterize the different parts of each study. One of the items is not scoreable in the field of sports science (item 1). Scores were independently calculated, avoiding any potential bias of the authors. When a study was not available on the PEDro databases, two authors alone (M.J. and A.M.) rated the risk of bias. Disagreements between authors were solved by consensus in a meeting with a third author (R.O.). When this was not achieved, a third investigator (R.O.) was used to carry out the analysis and debate with the first two investigators to reach an agreement.

Certainty Assessment
Based on the Physiotherapy Evidence Database scale and to assess the interventions' evidence, the [39] criteria were applied. Therefore, the selected studies were grouped by levels of evidence, according to their methodological quality. A study with a PEDro score of 6 or more is considered level 1 (high methodological quality) (6-8: good, 9-10: excellent), and a score of 5 or less is considered level 2 (low methodological quality) (4-5: moderate; <4: poor). Due to the clinical and statistical heterogeneity of the results, a qualitative review was performed, conducting a best-evidence synthesis [40,41]. This classification indicates that if the number of studies displaying the same level of evidence for the same outcome measure or equivalent is lower than 50% of the total number of studies found, no evidence can be concluded regarding any of the methods involved in the study.

Selection of Studies
A total of 258 studies were identified, through research carried out in the databases. In a first phase, which included the reading of titles and abstracts, 22 studies potentially relevant to the study were identified. Considering the previously defined eligibility criteria and after the full reading of the articles, 12 studies were identified as meeting the criteria for inclusion and were assessed for quality using the PEDro scale and included in this systematic review for full analysis. Figure 1 represents the flowchart of this systematic review.

Methodology Quality
The analysis of the quality of the 12 studies presents scores ranging between 4 and 7 on the PEDro scale, showing a moderate to good quality of the methodological procedures [37], as mentioned in Table 2. Items 5 and 6 were not applicable to the studies included.
Healthcare 2023, 11, x FOR PEER REVIEW 5 of 28 this systematic review for full analysis. Figure 1 represents the flowchart of this systematic review.

Methodology Quality
The analysis of the quality of the 12 studies presents scores ranging between 4 and 7 on the PEDro scale, showing a moderate to good quality of the methodological procedures [37], as mentioned in Table 2. Items 5 and 6 were not applicable to the studies included.

Studies Characteristics
The Table 3 presents the characteristics of the studies, namely: authors' names, year of publication, aims, participants, assessment instruments, duration/frequency, exercises, and intensities.
CCT is a form of exercise performed "continuously without any periods of rest involved". CCT usually involves cardiorespiratory activities (e.g., walking, running, cycling), in turn, ICT alternates shorts bursts of moderate to intense activity with longer intervals (about 1-2 min) of less intense activity. For example, if the exercise is walking, alternate with short runs [54][55][56].

Participants
From all selected studies, the total number of participants involved was 402, with 186 being included in the intervention groups and 192 in the control groups. The participants included children, adolescents, and adults. Specifically, there were two studies with child participants [44,45]. From the 12 studies selected, nine were carried out in the population with Down syndrome [42,[44][45][46][47][50][51][52][53], while only three were carried out with participants with ID [43,48,49].

CT Programs
All selected studies presented assessment protocols, namely the anthropometric assessment of weight and height, which were present in six studies [42,43,[45][46][47]51] or the assessment of body composition, such as calculating the BMI, measuring the perimeter of the waist, abdominal, and thigh, presented in six studies [42,43,46,50,51,53].
Only two studies [42,43] assessed neuromuscular capacity using a manual dynamometer. One study also applied the functional test of a 30 s chair stand [42].
CCT was carried out through walking, running, or using ergometers such as treadmills, steps, or stationary bikes, in which intensities vary from 70% to 80% VO 2 peak , 100% to 110% of the ventilatory threshold or between 50% and 75% HR max . All studies started the CCT program with low (very light to light) intensity, with the exception of the study by Boer and Moss [42] which started with moderate intensity. All studies prescribed a progressive increase in intensity, (low to moderate and/or moderate to vigorous), with the exception of the studies by Holzapfel [46,47] and Chen [44] where there is no intensity progression.
Regarding the body composition effects of CCT, there was a reduction in body weight, percentage of fat mass, waist circumference, and waist-to-hip-ratio, as shown in Table 4 and Appendix A. Table 4. Percentage change in anthropometric variables with CCT programs intervention.

Interval Cardiorespiratory Training and Main Results
Considering the ICT method, several variables showed improvements which were presented in Table 8 and in Appendix A.
The study by El Kafy and Helal [45] was performed with children participants (8 to 12 years), showing that this age group can also improve their cardiorespiratory function, namely: vital capacity, forced vital capacity, forced expiratory volume, and peak expiratory flow rate. The studies selected in this review had the following characteristics in ICT: a shorter volume with a duration of 10 s at maximum speed, followed by 90 s of rest [42] or 15 s of full speed with 45 s of rest [43] or 2 min of work for 1 min of rest [45]. In the Boer et al. [43] study, intensity was not quantified, while Boer and Moss [42] used an intensity of 100% of the ventilatory threshold (aerobic threshold), increased up to 110% (anaerobic threshold), and El Kafy and Helal [45] carried out a prescription based on the VO 2 peak , specifically between 70% to 80% VO 2 peak .
The most common parameters used for the prescription and control of the effort intensity were the % HR max , with percentages ranging from 50% to 80%; however, a prescription based on VO 2max (70% to 80%) or ventilatory threshold (100% to 110%) were also applied [42,43,45].

Discussion
The present study aimed to describe the effects on the health-related and functional capacity outcomes of CT for individuals with ID as well as to characterize CT programs implemented in these individuals and the type of exercise and the guidelines for the prescription of effective CT programs.
From the 12 studies analyzed, two involved children as participants and demonstrated that they, too, could improve cardiorespiratory function [45]. In addition to promoting cardiorespiratory function, the literature shows that CT in children also improves lipid profile, hemodynamic parameters, and metabolic markers [57].
CT also promotes improvements in neuromuscular capacity of upper and lower limbs [42,43]. Neuromuscular capacity was assessed using a manual dynamometer or functional tests such as sit-to-stand [42,43]. Boer and Moss [42] and Boer et al. [43] reported an increase in neuromuscular capacity, especially in the CCT group. Our results are supported in the literature namely by the Konopka and Harber [60] study where authors reported that CT alters protein metabolism and induces skeletal muscle hypertrophy. These findings are important when prescribing a physical exercise program, to achieve maximum benefits.
CT seems to be the best training method to improve some variables such as those indicated in Tables 4-8 and Appendix A [61]. Since these variables were associated with the onset of cardiovascular and metabolic diseases [62,63], their improvement through CT seemed particularly relevant. In recent decades, there has been a significant increase in the years of life expectancy of individuals with ID and with Down syndrome, justifying the greater need to study the effects of intervention strategies that improve health and reduce the impact of comorbidities associated with ageing [64]. According to the results of several studies, the CT seems to be an effective type of exercise in people with ID.

Exercise Prescription
Considering the characterization of CT programs of all studies included in the present systematic review, there were aspects that are common and more evident, such as: (a) duration of 12 weeks; (b) three sessions per week; (c) duration of 20 to 60 min per session, always encompassing the warm-up and cool down phases; (d) exercises performed using ergometers such as cycling exercise, elliptical, stepper, or treadmill walking; (e) intensity between 50% and 80% of HR max or 70% to 80% VO 2max .
The ACSM [54] most recent recommendations for CT prescription for the population with ID and Down syndrome show an intensity of 40% to 80% of VO 2max or HR max , 30 to 60 min per session, suggesting activities like walking-based activities and swimming ergometry (arm and leg). The characteristics of the applied intervention programs included in this systematic review were in accordance with international recommendations, namely the ACSM [54] and the National Strength and Conditioning Association-NSCA guidelines [65]. All studies have prescribed intensities recommended by the ACSM [54]; however, all studies started the CT programs at intensity values higher than those recommended by these guidelines. Considering the heterogeneity of the population with ID, the prescription of training intensity may be related to the physiological characteristics of the individuals, namely if they also have Down syndrome or depending on the degree of disability (mild, moderate, severe, and/or profound).
The duration of the CT program interventions analyzed varied between 8 and 12 weeks [42,[44][45][46][47][48][49][50][51][52][53]. However, Rodrigues et al. [66], by analyzing the effect of past behavior on future behavior, considering the motivational sequence proposed by self-determination theory, points out that, in terms of adherence and maintenance of a physical exercise behavior, the first 6 months of participation are crucial for the success of the following 6 months. This systematic review reveals a lack of studies with longer duration (six or more months), which is an aspect to be considered in future intervention studies.

Continuous Cardiorespiratory Training vs. Interval Cardiorespiratory Training
The literature showed that two CT methods such as CCT and ICT, can be prescribed for individuals with ID and considered as safe and effective options, given the absence of adverse events, the low dropout rate and excellent adherence to training. Although several studies have implement CCT [42,43,46,47,[50][51][52][53], the ICT may be more effective, particularly for individuals with some training experience, since this is a method with higher intensity [42,43]. Nonetheless, CCT is the most recommended by ACSM [54] for the population with ID and Down syndrome. Three days or more of moderate to vigorous CT, 40-80% VO 2 peak , for 30 to 60 min, using walking, ergometry, or other activities is recommended.
Results of the present systematic review were supported by other studies which showed that exercise intensity is an important factor for the improvement of cardiorespiratory function and reversing the risk factors of the metabolic syndrome [67,68]. A recent meta-analysis [69], compared the use of ICT and CCT methods. ICT results showed a greater increase in peak oxygen uptake, peak heart rate, first ventilatory threshold, and a reduced ejection fraction compared with CCT, in patients with coronary artery disease or heart failure. Another meta-analysis reported a more significant increase in VO 2max in ICT when compared with CCT, in healthy, young to middle-aged adults [70]. However, it appears to be more exhausting and stressful for individuals with ID which appear to have a lower degree of resilience to the stress imposed by physical exertion [42,43]. Although the present systematic review was not able to find which type of CT is better, ICT due to the higher exertion intensities would provide better results which should be analyzed in future studies with ID and/or Down syndrome participants.

Physiological Process
During cardiorespiratory training, several physiological processes occur, leading to various physiological adaptations in the human body. With exercise, the human body needs more oxygen in the muscles. To respond to this demand, there is an increase in heart rate, ensuring that the heart pumps more blood. With this physiological response, we expect an increase in cardiac output: the amount of blood pumped per heartbeat. To allow greater blood flow to the muscles, the blood vessels dilate, allowing for increased blood flow (oxygen and nutrients needed for activity). In turn, for greater oxygen uptake, lung ventilation increases. During exercise, energy expenditure increases, also increasing heat production. To keep the body at a healthy temperature, the body responds by sweating. Regular cardiorespiratory training, by triggering this whole process, affects cardiorespiratory capacity and can lead to the other adaptations mentioned above [54].

Limitations and Future Research
The authors of the studies included in this systematic review highlight some limitations found in their studies, which should be taken into account for future studies, such as lack of information or analysis regarding the level of DI [42]; difficulties in randomization [43,46,52]; associated comorbidities (e.g., cardiovascular diseases) [43]; lack of validity and reliability of some applied tests [43]; lack of quantification of physical activity practice [44]; small sample size [44,49]; large age range [49]; short duration of the intervention program [51]; lack of analysis of intervention detraining [51,52]; and measures of assessment susceptible to media errors [53].
This systematic review shows a lack of studies on the effects of applying a CT program in individuals with ID but without another associated conditions. At the same time, no intervention studies were found for the elderly population with ID which leads us to suggest the application of CT programs in older people with ID. Although the ACSM [54] does not distinguish between age groups, it will be interesting in the future to realize that the guidelines and benefits are transversal for all. Equally, more randomized studies are needed to assess the variables shown in Tables 4-8 and in non-randomized controlled trials studies since their programs are quite different which difficult comparisons between studies. The longer implementation of CT programs will also allow the knowledge enlightenment regarding training methods, programs structure, type of exercise, and periodization in order to have more adapted and effective exercise prescriptions, as some of the barriers to physical activity are also reduced [26]. Although we know that individuals with Down syndrome have different physiological responses than individuals with just ID due to an underlying autonomic dysfunction [71] and taking into account the heterogeneity of assessment methodologies and variables evaluated, we cannot conclude whether the results are different in such individuals. However, the ACSM [54] does not make this differentiation either. It is important to take special care in the prescription and implementation of CT programs in the population with Down syndrome, due to its atlantoaxial instability [72]. To increase physical fitness, namely cardiorespiratory fitness or VO 2max , Swain and Franklin [73] suggested that the intensity of the exercise should vary according to the participant initial fitness level.
The present systematic review showed some limitations similar to those recently reported by Jacinto et al. [74] concerning strength training for individuals with ID, such as (i) heterogeneity of different studies; (ii) little clearness in some studies regarding the randomization process; (iii) absence of follow-up; (iv) different assessment methodologies which did not allow further discussion or a meta-analysis about the CT effects produced; and (v) the level of ID was not mentioned in all studies included, which limits the generalization of the results and recommends such description in future studies.

Practical Implications
The present study includes aspects and recommendations that PE professionals should consider when structuring, prescribing, and implementing a CT program. For a population where a sedentary lifestyle prevails, with several associated comorbidities, the characteristics presented in this document become essential to promote the expected benefits and results, namely the maintenance/increase of physical fitness, quality of life, and health, thus decreasing, the risk of onset of chronic diseases. Along with the ACSM recommendations, to which this document is intended to be a supplement, the conditions for successful evaluation, prescription, implementation, and follow-up of CT in individuals with ID are met.
Associated with an appropriate lifestyle, the implementation of CT programs, incorporated into the routine of the target population, provokes a set of adaptations and benefits, promoting healthy aging and fuller health.

Conclusions
This manuscript includes a review of studies published in recent years about an indepth analysis of the basic guidelines for prescribing CT in individuals with ID and Down syndrome, and about its main benefits for health and well-being. In summary, the basic aspects for CT prescription are: (i). Duration of 8 to 12 weeks (we emphasize that the essential is that the CT programs are implemented continuously); (ii). Frequency of three sessions per week; (iii). Duration of 20 to 60 min per session, always taking into account the warm-up and cool down phases; (iv). Exercises performed using ergometers such as cycling exercise, elliptical, stepper, or treadmill walking; (v). Intensity between 50% to 80% of HR max or 70% to 80% VO 2max .
Although CCT is more frequently prescribed and recommended, ICT also seems to be a good option and more effective in variables such as peak oxygen uptake, peak heart rate, first ventilatory threshold, and a reduced ejection fraction. However, it should only be prescribed with some previous training experience, as it is a more exhausting and intense training method.
This systematic review also shows that CT promotes benefits in cardiorespiratory function, lipid profile, and hemodynamic and metabolic markers which have direct effects on body composition, as well as an increase in upper and lower limb strength and cognitive/neural capacity in individuals with ID and inclusive Down syndrome.

Data Availability Statement:
The data presented in this study are available on request from the corresponding author.

Conflicts of Interest:
The authors declare no conflict of interest.